Recruitment processes in long-lived species with delayed maturity: estimating key demographic parameters

Long-lived species show delayed maturity and generally skip breeding sites on a given year, causing difficulties in estimating demographic parameters. A novel multi-state capture – recapture model (model G for general) is proposed to estimate survival and recruitment. Model G considers long and short periods of non-attendance at the breeding site. Model G is compared against a reduced model (model R) to test if pre-breeders skip the studied site a given year, potentially prospecting other breeding habitats.
This model is applied to the vulnerable Cory's shearwaters seabird species. As for many species, natal philopatry, pre-breeding attendance and prospecting play an important role for recruitment into the breeding population. Model G shows that all Cory's shearwaters come back to their natal colony, and attend the colony before recruiting into the breeding population. Moreover, model G is preferred against model R, highlighting that prospecting plays a potentially role in the recruitment processes. Return and recruitment probabilities show similar time variation, suggesting an environmental forcing. The maximum probability of the first breeding is reached at the age of seven years. During the first year the annual survival rate is 0.52 (IC_95%=[0.40, 0.64]) and pre-breeders and adult annual survival rates do not differ, being respectively 0.88, IC_95%=[0.83, 0.92] and 0.89, IC_95%=[0.88, 0.9].
Model G provides an improvement to estimate demographic parameters for long-lived species life cycle and an adequate framework to test the influence of covariates. Model G is structured by age and breeding status categories, allowing easy further population models.     

Stress associated with group living in a long-lived bird

Many long-lived avian species adopt life strategies that involve a gregarious way of life at juvenile and sub-adult stages and territoriality during adulthood. However, the potential associated costs of these life styles, such as stress, are poorly understood. We examined the effects of group living, sex and parasite load on the baseline concentration of faecal stress hormone (corticosterone) metabolites in a wild population of common ravens (Corvus corax). Corticosterone concentrations were significantly higher in non-breeding gregarious ravens than in territorial adults. Among territorial birds, males showed higher stress levels than their mates. Parasite burdens did not affect hormone levels. Our results suggest a key role of the social context in the stress profiles of the two population fractions, and that group living may be more energetically demanding than maintaining a territory. These findings have implications for understanding hormonal mechanisms under different life styles and may inspire further research on the link between hormone levels and selective pressures modulating gregarious and territorial strategies in long-lived birds.     

Pre-fledgling oxidative damage predicts recruitment in a long-lived bird

Empirical evidence has shown that stressful conditions experienced during development may exert long-term negative effects on life-history traits. Although it has been suggested that oxidative stress has long-term effects, little is known about delayed consequences of oxidative stress experienced early in life in fitness-related traits. Here, we tested whether oxidative stress during development has long-term effects on a life-history trait directly related to fitness in three colonies of European shags Phalacrocorax aristotelis. Our results revealed that recruitment probability decreased with oxidative damage during the nestling period; oxidative damage, in turn, was related to the level of antioxidant capacity. Our results suggest a link between oxidative stress during development and survival to adulthood, a key element of population dynamics.     

Characterising demographic contributions to observed population change in a declining migrant bird

Populations of Afro‐Palearctic migrant birds have shown severe declines in recent decades. To identify the causes of these declines, accurate measures of both demographic rates (seasonal productivity, apparent survival, immigration) and environmental parameters will allow conservation and research actions to be targeted effectively. We used detailed observations of marked breeding birds from a ‘stronghold’ population of whinchats Saxicola rubetra in England (stable against the declining European trend) to reveal both on‐site and external mechanisms that contribute to population change. From field data, a population model was developed based on demographic rates from 2011 to 2014. Observed population trends were compared to the predicted population trends to assess model‐accuracy and the influence of outside factors, such as immigration. The sensitivity of the projected population growth rate to relative change in each demographic rate was also explored. Against expectations of high productivity, we identified low seasonal breeding success due to nocturnal predation and low apparent first‐year survival, which led to a projected population growth rate (λ) of 0.818, indicating a declining trend. However, this trend was not reflected in the census counts, suggesting that high immigration was probably responsible for buffering against this decline. Elasticity analysis indicated λ was most sensitive to changes in adult survival but with covariance between demographic rates accounted for, most temporal variation in λ was due to variation in productivity. Our study demonstrates that high quality breeding habitat can buffer against population decline but high immigration and low productivity will expose even such stronghold populations to potential decline or abandonment if either factor is unsustainable. First‐year survival also appeared low, however this result is potentially confounded by high natal dispersal. First‐year survival and/or dispersal remains a significant knowledge gap that potentially undermines local solutions aimed at counteracting low productivity.     

Adjustment of the annual cycle to climatic change in a long-lived migratory bird species

Climate change has advanced the phenology of many organisms. Migratory animals face particular problems because climate change in the breeding and the wintering range may be asynchronous, preventing rapid response to changing conditions. Advancement in timing of spring migration may have carry-over effects to other parts of the annual cycle, simply because advancement of one event in the annual cycle also advances subsequent events, gradually causing a general shift in the timing of the entire annual cycle. Such a phenotypic shift could generate accumulating effects over the years for individuals, but also across generations. Here we test this novel hypothesis of phenotypic response to climate change by using long-term data on the Arctic tern Sterna paradisaea. Mean breeding date advanced by almost three weeks during the last 70 years. Annual arrival date at the breeding grounds during a period of 47 years was predicted by environmental conditions in the winter quarters in the Southern Ocean near the Antarctic and by mean breeding date the previous year. Annual mean breeding date was only marginally determined by timing of arrival the current year, but to a larger extent by arrival date and breeding date the previous year. Learning affected arrival date as shown by a positive correlation between arrival date in year (i+1) relative to breeding date in year (i) and the selective advantage of early breeding in year (i). This provides a mechanism for changes in arrival date being adjusted to changing environmental conditions. This study suggests that adaptation to changing climatic conditions can be achieved through learning from year to year[Current Zoology 55(2):92-101,2009].     

Experimentally delayed hatching triggers a magnified stress response in a long-lived bird

In birds, the timing of breeding is a key life-history trait with crucial fitness consequences. We predicted that parents may value a brood less if it hatched later than expected, thereby decreasing their parental effort. In addition, breeding effort would be further modulated by the age-specific decline of future breeding opportunities. We experimentally investigated whether snow petrels, Pagodroma nivea, were less committed to care for a chick that hatched later than expected. The timing of hatching was manipulated by swapping eggs between early and late known-age pairs (7-44 years old), and investigations on hormonal and behavioral adjustments were conducted. As a hormonal gauge of parental commitment to the brood, we measured the corticosterone stress response of guarding adults. Indeed, an acute stress response mediates energy allocation towards survival at the expense of current reproduction and is magnified when the current brood value is low, as it is expected to be in young and/or delayed parents. As predicted, egg desertion and the magnitude of the stress response was stronger in delayed pairs compared to control ones. However, the treatment did not decrease the length of the guarding period, chick condition and chick survival. In addition, old parents resisted stress better (lower stress-induced corticosterone levels) than young ones. Our study provides evidence that snow petrels, as prudent parents, may value a brood less if it hatched later than expected. Thus, in long-lived birds, the responsiveness to stressors appeared to be adjusted according to the individual prospect of future breeding opportunities (age) and to the current brood value (timing of breeding).     

Short- and long-term consequences of individual and territory quality in a long-lived bird

Site-quality is a major determinant of fitness but its effect can be confounded by individual quality, a relationship that has been little studied in large, long-lived vertebrates. The fitness effects of quality estimates depend on the assumption of co-variation between individual and territory quality and can be framed as five working hypotheses: no effect on fitness, exclusive effect of individual quality, exclusive effect of site quality, and independent or interactive effects of the two. We explored such a framework using a medium-sized raptor, the black kite Milvus migrans, as a model species. Individual and territory quality co-varied, but the strength of the relationship varied across different estimates of individual quality (age, body size, or mass residuals). Short-term production of fledglings was related to the independent effects of both individual and territory quality. However, longer-term production of recruits was related solely to territory quality. The disappearance of individual quality effects over the long-term may be caused by antagonistic selective pressures acting during different stages of the life cycle. Our results contribute to a growing appreciation of the long-term fitness-benefits of advantages experienced in early life and highlight the importance of a long-term perspective in studies assessing the effects of individual and territory quality. In our case study, prioritizing sites for conservation on the basis of territory quality may be a feasible pathway to maintain the viability of the population. However, scenarios where such a method could be inefficient have been previously reported, suggesting caution in its application. More studies are needed to understand the generality of the efficiency of priority-setting approaches based on site quality.     

Social information in nest colonisation and occupancy in a long-lived, solitary breeding bird

Recent work increasingly reveals the importance of social information in individual dispersal decisions, population dynamics and conservation. Much of the knowledge gained to date comes from studies on short-lived and/or densely breeding species. In contrast, our understanding of the processes involved in nest-site selection for long-lived, solitary breeding species is insufficient. We increased nest-site availability by nest-box supplementation over a 5-year period in a population of a long-lived, solitary, secondary-cavity nesting bird, the European roller Coracias garrulus, breeding in natural cavities and human constructions. We tested the nest limitation and the inadvertent conspecific social information hypothesis in order to study the dynamics and mechanisms of abandonment of previously used nests and the colonisation of new ones. Our data lend support to the nest-limitation hypothesis both in terms of quantity-population and the size of breeding clusters increased, and suitability--the majority of pairs used and re-occupied nest-boxes. Nevertheless, the use of natural cavities did not decrease after 5 years. At the between-patch scale, rollers were revealed to colonise nest-boxes based on conspecific social attraction, namely distance to the nearest neighbour in the same season. Despite the unpredictability of patch productivity, at the within--patch scale, the selection of previously unoccupied cavities was consistent with the performance-based conspecific attraction hypothesis. Philopatry could account for the repeated use of cavities, because nests that were used for two successive years were more likely to also be reused in the subsequent season.     

Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird

We tested the hypothesis that parental effort modulates the magnitude of corticosterone and prolactin responses to stress in a long-lived bird, the Black-legged kittiwake (Rissa tridactyla). To do so, we compared corticosterone and prolactin responses to capture/restraint stress between chick-rearing birds and failed breeders (no parental effort). We predicted that (1) the increase in plasma corticosterone levels in response to stress should be lower in chick-rearing birds, (2) the decrease in plasma prolactin levels in response to stress should be lower in chick-rearing birds, and (3) as both sexes care for the chick, there should be no sex difference in the hormonal response to stress. Baseline plasma corticosterone and prolactin levels were higher in chick-rearing birds and were not influenced by body condition. Failed breeders were in better condition than chick-rearing individuals. Corticosterone response to stress was unaffected by parental effort as both chick-rearing and failed birds exhibited a robust corticosterone increase. Prolactin response to stress was however clearly influenced by parental effort: chick-rearing birds showed a modest 9% prolactin decrease whereas in failed birds prolactin concentrations fell by 41%. Body condition did not influence hormonal responses to stress. When facing stressful condition, breeding kittiwakes attenuate their prolactin response to stress while enhancing their secretion of corticosterone. Increasing corticosterone secretion triggers foraging efforts and diminishes nest attendance whereas an attenuation of prolactin response to stress maintains parental behavior. We suggest that this hormonal mechanism facilitates a flexible time-budget that has been interpreted as a buffer against environmental variability.     

Differences in home-range sizes of a bird species in its original,refuge and substitution habitats: challenges to conservation in anthropogenic habitats

In the current context of the anthropocene, the original habitats of many species have been modified or destroyed. Animals may be forced to move from their original habitats, either to refuge habitats that are suboptimal natural habitats, or to substitution habitats that are anthropogenic. The quality of refuge habitats may be lower than that of the original ones, whereas substitution habitats may be of a similar or even better quality. Here, we test this hypothesis empirically, using the example of coastal populations of the bluethroat, Luscinina svecica namnetum. In a radio-tracking survey, we compared the home-range sizes (considered here a proxy of habitat quality) of the breeding males in their original (coastal saltmarshes), refuge (inland reedbeds) and substitution (coastal salinas) habitats. We found that home ranges are up to 15 times larger in the substitution habitat than in the original one, and intermediate in the refuge habitat, suggesting that substitution habitats have the lowest quality and original habitats the highest. To date, most studies and conservation programs related to this species have focused on its substitution habitats. This result challenges the interest of focusing on anthropogenic habitats when studying and conserving such a species, because such habitats may only be low-quality substitutes.     

Migratory connectivity in a declining bird species: using feather isotopes to inform demographic modelling

Aim Conservation programmes for endangered migratory species or populations require locating and evaluating breeding, stopover and wintering areas. We used multiple stable isotopes in two endangered European populations of wrynecks, Jynx torquilla L., to locate wintering regions and assess the degree of migratory connectivity between breeding and wintering populations. Location Switzerland and Germany. Methods We analysed stable nitrogen (δ¹⁵N), carbon (δ¹³C) and hydrogen (δD) isotopes from wing feathers from two populations of wrynecks to infer their wintering origins and to assess the strength of migratory connectivity. We tested whether variation in feather isotopic values within the Swiss population was affected by bird age and collection year and then considered differences in isotopic values between the two breeding populations. We used isotopic values of summer‐ and winter‐grown feathers to estimate seasonal distributions. Finally, we calculated a species‐specific δD discrimination factor between feathers and mean annual δD values to assign winter‐grown feathers to origin. Results Bird age and collection year caused substantial isotopic variation in winter‐grown feathers, which may be because of annually variable weather conditions, movements of birds among wintering sites and/or reflect asynchronous moulting or selection pressure. The large isotopic variance in winter‐grown feathers nevertheless suggested low migratory connectivity for each breeding population, with partially overlapping wintering regions for the two populations. Main conclusions Isotopic variance in winter‐grown feathers of two breeding populations of wrynecks and their geographical assignment point to defined, albeit overlapping, wintering areas, suggesting both leapfrog migration and low migratory connectivity. On this basis, integrative demographic models can be built looking at seasonal survival patterns with links to local environmental conditions on both breeding and wintering grounds, which may elucidate causes of declines in migratory bird species.     

Variations in bird abundance in tropical arid and semi-arid habitats

Temporal variation in bird abundance was studied during a complete annual cycle in a thorn scrub, a thorn woodland and a deciduous forest in northeastern Venezuela. Abundance of site-attached and transient birds from different feeding guilds was determined by mist-netting at 2-week intervals. Diets were investigated by regurgitated samples. The overall avifauna was characterized by a low number of species but they were present all year despite showing strong seasonal fluctuations in abundance. The number of bird species and individuals peaked before and after the reproductive period. These high values probably were associated with movement of species feeding on plant food during the late dry season and the post-breeding dispersion of juveniles. Bird richness and abundance were lowest during the breeding season and in the early dry season when food abundance was low. Birds from different feeding guilds showed distinct patterns of seasonal abundance which tended to be similar at all three sites. Transient birds represented a large portion of the avifauna, particularly in nectarivores, frugivores and granivores during the dry season. We used a canonical correspondence analysis to demonstrate that bird abundance was correlated with breeding activity, rainfall seasonality and food abundance, with the influence of each parameter varying according to feeding guilds, spatial behaviour of individuals and habitats. Despite a great turnover in the occurrence of the diverse food types available, species composition remained strikingly constant during the year, with birds responding to seasonal changes primarily through a generalist feeding habit and a highly variable rate of transience.     

Plastome organization and evolution of chloroplast genes in Cardamine species adapted to contrasting habitats

Background

Plastid genomes, also known as plastomes, are shaped by the selective forces acting on the fundamental cellular functions they code for and thus they are expected to preserve signatures of the adaptive path undertaken by different plant species during evolution. To identify molecular signatures of positive selection associated to adaptation to contrasting ecological niches, we sequenced with Solexa technology the plastomes of two congeneric Brassicaceae species with different habitat preference, Cardamine resedifolia and Cardamine impatiens.

Results

Following in-depth characterization of plastome organization, repeat patterns and gene space, the comparison of the newly sequenced plastomes between each other and with 15 fully sequenced Brassicaceae plastomes publically available in GenBank uncovered dynamic variation of the IR boundaries in the Cardamine lineage. We further detected signatures of positive selection in ten of the 75 protein-coding genes of the examined plastomes, identifying a range of chloroplast functions putatively involved in adaptive processes within the family. For instance, the three residues found to be under positive selection in RUBISCO could possibly be involved in the modulation of RUBISCO aggregation/activation and enzymatic specificty in Brassicaceae. In addition, our results points to differential evolutionary rates in Cardamine plastomes.

Conclusions

Overall our results support the existence of wider signatures of positive selection in the plastome of C. resedifolia, possibly as a consequence of adaptation to high altitude environments. We further provide a first characterization of the selective patterns shaping the Brassicaceae plastomes, which could help elucidate the driving forces underlying adaptation and evolution in this important plant family.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1498-0) contains supplementary material, which is available to authorized users.     

Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird

There is compelling evidence about the manifest effects of inbreeding depression on individual fitness and populations' risk of extinction. The majority of studies addressing inbreeding depression on wild populations are generally based on indirect measures of inbreeding using neutral markers. However, the study of functional loci, such as genes of the major histocompatibility complex (MHC), is highly recommended. MHC genes constitute an essential component of the immune system of individuals, which is directly related to individual fitness and survival. In this study, we analyse heterozygosity fitness correlations of neutral and adaptive genetic variation (22 microsatellite loci and two loci of the MHC class II, respectively) with the age of recruitment and breeding success of a decimated and geographically isolated population of a long-lived territorial vulture. Our results indicate a negative correlation between neutral genetic diversity and age of recruitment, suggesting that inbreeding may be delaying reproduction. We also found a positive correlation between functional (MHC) genetic diversity and breeding success, together with a specific positive effect of the most frequent pair of cosegregating MHC alleles in the population. Globally, our findings demonstrate that genetic depauperation in small populations has a negative impact on the individual fitness, thus increasing the populations' extinction risk.     

Jaatha: a fast composite-likelihood approach to estimate demographic parameters

While information about a species’ demography is interesting in its own right, it is an absolute necessity for certain types of population genetic analyses. The most widely used methods to infer a species’ demographic history do not take intralocus recombination or recent divergence into account, and some methods take several weeks to converge. Here, we present Jaatha, a new composite‐likelihood method that does incorporate recent divergence and is also applicable when intralocus recombination rates are high. This new method estimates four demographic parameters. The accuracy of Jaatha is comparable to that of other currently available methods, although it is superior under certain conditions, especially when divergence is very recent. As a proof of concept, we apply this new method to estimate demographic parameters for two closely related wild tomato species, Solanum chilense and S. peruvianum. Our results indicate that these species likely diverged 1.44·N generations ago, where N is the effective population size of S. chilense, and that some introgression between these species continued after the divergence process initiated. Furthermore, S. peruvianum likely experienced a population expansion following speciation.